Invasive Stink Bugs and Related Species (Pentatomoidea)

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Halyomorpha halys (Stål) 275


in orchards were various species of tettigoniids and carabid beetles followed by earwigs, salticid spiders,
and crickets (gryllids). In contrast, generalist predators often found in vegetable and field crops, such as
coccinellids, anthocorids, and predatory pentatomids, were the most important predators of H. halys
eggs in those habitats. In the case of Orius insidiosus Say, Fraga et al. (2016) found in greenhouse, labo-
ratory, and field experiments that adults were attracted to tridecane, a plant volatile released in response
to feeding by H. halys. However this attraction did not result in increased predation indicating that it
might be acting as an arrestant. In a separate study involving parasitoids, Rondoni et al. (2017) showed
that native egg parasitoids can exploit volatiles emitted by H. halys and by Vicia faba L. in response to
feeding by H. halys. Clearly, native predators of many types may play an important role in helping to
reduce stink bug populations, especially in conservation biological control where agricultural systems
may be manipulated in various ways to enhance predator populations.
Limited work has been published to date regarding pathogens. One strain (GHA) of the entomopatho-
genic fungus Beauvaria bassiana (Bals.-Criv) Vuill., which is the active ingredient in Botanigard®, and
several other tested strains showed strong efficacy against adults of Halyomorpha halys in laboratory trials
(Gouli et al. 2012). Strains of Metarhizium anisopliae (Metchsnikoff) Sorokin were less efficacious (Gouli
et al. 2012, Pike 2014), and there is evidence that defensive compounds released by this bug, including
trans-2-octenal and trans-2-decenal, may inhibit fungal growth and prevent spore germination at low con-
centrations (Pike 2014). Evidence of microsporidian infections of H. halys has also recently been found in
assays conducted to determine the cause of laboratory colony die-offs. Following the discovery of labora-
tory infections, microsporidians also have been detected in some field populations, and further research is
needed to determine their frequency and impact (Ann Hajek, unpublished data; see Acknowledgments).
Several species of tachinid flies in North America, which are parasitoids of other pentatomid species,
have been reported to respond to their host pheromones and were attracted to field lures containing the
pheromones (Aldrich et al. 2006); these authors reared several specimens of Trichopoda pennipes ( F.)
from field-collected Halyomorpha halys. The native tachinid fly Euclytia flava (Townsend) also was
found in traps baited with commercial H. halys pheromone lures in California surveys (Lara et al. 2016).
The flies deposit their eggs on dorsal and/or ventral surfaces of H. halys adults which then hatch and
penetrate into the stink bug hosts; however, successful development and emergence rates have been low
(Rice et al. 2014), which suggest that although the flies recognize the stink bugs as a potential hosts, the
bugs are somehow physiologically unsuitable.
Because egg masses can be difficult to locate in the field, sentinel egg masses also have been used in
many studies to document the levels of parasitism of stink bug eggs and species diversity of indigenous
egg parasitoids in various habitats and crops in the United States and in Europe. Species of Anastatus
( Eupel m idae), Trissolcus, and Telenomus (Scelionidae) have been the most commonly encountered hyme-
nopterous parasitoids reared from wild (naturally laid) and sentinel Halyomorpha halys eggs, with occa-
sional recoveries of Ooencyrtus (Encyrtidae) (e.g., Ooencyrtus telenomicida Vassiliex in Europe) and
Gryon (Scelionidae in the United States). Parasitism rates by Anastatus reduvii (Howard), Anastatus
pearsalli Ashmead, and Anastatus mirabilis (Walsh and Riley) in the United States and Anastatus bifasci-
atus (Geoffroy) in Europe; Trissolcus brochymenae (Ashmead), Trissolcus edessae Fouts, Trissolcus eus-
chisti (Ashmead), Trissolcus hullensis (Harrington), Trissolcus thyantae Ashmead, Trissolcus utahensis
(Ashmead) (as Telenomus utahensis Ashmead) in the United States, and Telenomus podisi Ashmead and
Telenomus persimilis Ashmead in North America generally are low – well under 10% (Rice et al. 2014,
Cornelius et al. 2016, Ogburn et al. 2016, Roversi et al. 2016, Dieckhoff et al. 2017). Furthermore, notable
variation appears to exist in the proportion of successful development of some geographic populations of
native parasitoids on H. halys, with some populations having a complete inability to develop to emergence
(e.g., Telenomus podisi in Ontario, Canada [Abram et al. 2014]). Although the native parasitoids often fail
to develop, they may nevertheless attack and deposit eggs, causing elevated levels of mortality to the host
eggs (Abram et al. 2014, Haye et al. 2015a, Cornelius et al. 2017, Dieckhoff et al. 2017). However, when
sentinel egg masses were frozen prior to field placement, the successful development of native parasitoids
was increased, sometimes considerably (Haye et al. 2015a, Herlihy et al. 2016). In some cases, the use of
frozen eggs permitted the successful development of parasitoid species that were not able to develop in
fresh H. halys eggs (Haye et al. 2015a). Presumably the freezing process disables whatever physiological
defensive barriers exist in fresh eggs. Indirect evidence of this has been shown by Tognon et al. (2016).

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